Abstract
Background: Despite the effectiveness of a two-stage exchange protocol for the treatment of deep periprosthetic infection, infection can persist after resection arthroplasty and treatment with antibiotics, leading to a failed second-stage reconstruction. Intraoperative analysis of frozen sections has been shown to have a high sensitivity and specificity for the identification of infection at the time of revision arthroplasty; however, the usefulness of this test at the time of reoperation after resection arthroplasty and treatment with antibiotics is, to our knowledge, unknown.Methods: The medical records of sixty-four consecutive patients who had had a resection arthroplasty of either the knee (thirty-three patients) or the hip (thirty-one patients) and had had intraoperative analysis of frozen sections of periprosthetic tissue obtained at the time of a second-stage operation were reviewed. The mean interval between the resection arthroplasty and the attempted reimplantation was nineteen weeks. The results of the intraoperative analysis of the frozen sections were compared with those of analysis of permanent histological sections of the same tissues and with those of intraoperative cultures of specimens obtained from within the joint. The findings of the analyses of the frozen sections and the permanent histological sections were considered to be consistent with acute inflammation and infection if a mean of ten polymorphonuclear leukocytes or more per high-power field (forty times magnification) were seen in the five most cellular areas.Results: The intraoperative frozen sections of the specimens from two patients (one of whom was considered to have a persistent infection) met the criteria for acute inflammation. Four patients were considered to have a persistent infection on the basis of positive intraoperative cultures or permanent histological sections. Overall, intraoperative analysis of frozen sections at the time of reimplantation after resection arthroplasty had a sensitivity of 25 percent (detection of one of four persistent infections), a specificity of 98 percent, a positive predictive value of 50 percent (one of two), a negative predictive value of 95 percent, and an accuracy of 94 percent.Conclusions: A negative finding on intraoperative analysis of frozen sections has a high predictive value with regard to ruling out the presence of infection; however, the sensitivity of the test for the detection of persistent infection is poor.
Infection at the site of a total hip or knee arthroplasty is a devastating complication. Despite a reduction in the rate of infection associated with reconstructive procedures in adults, given the increase in the total number of arthroplasties performed yearly and in the longevity of these devices in vivo the absolute number of periprosthetic infections will inevitably increase27. Two-stage exchange arthroplasty has been reported to be the most successful procedure for the treatment of periprosthetic infection; in a total group of 401 infected knees from sixteen studies14, infection was eradicated in 85 percent, and in a total group of 581 infected hips from twenty studies13, infection was eradicated in 89 percent.
Whereas a large body of information is available regarding the diagnosis and initial treatment of deep infection, few guidelines are available for determining when it is suitable to attempt reimplantation after a resection arthroplasty has been performed for the treatment of infection. Intraoperative analysis of frozen sections is a reliable indicator of infection during revision hip or knee arthroplasty2,7,12,18,22, and the procedure has been suggested as a method for determining the suitability of a previously infected site for prosthetic reimplantation10,13,15,16,25,32,33. However, the ability of intraoperative analysis of frozen sections to detect persistent infection or to correctly demonstrate that a previous infection was treated adequately has not been analyzed specifically, to our knowledge, as patients who were being managed with a second-stage reconstruction have been excluded from previous studies of the reliability of this technique2,12,18.
The purpose of the current study was to determine the role of analysis of frozen sections at the time of reoperation after resection arthroplasty of the hip or knee for the treatment of deep infection. The ability to assess intraoperatively the suitability of a previously infected site for prosthetic reimplantation would help the orthopaedic surgeon to optimize the care of these patients.
*No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. Funds were received in total or partial support of the research or clinical study presented in this article. The funding source was the Ann and Harry J. Reicher, Foundation.
†Musculoskeletal Research Center, Room 1500, Department of Orthopaedic Surgery, New York University Hospital for Joint Diseases, 301 East 17th Street, New York, N.Y. 10003. E-mail address for Dr. Della Valle:craigd@yahoo.com. E-mail address for Dr. Di Cesaere: pedicesare@aol.com.
‡Department of Pathology, Hospital for Joint Diseases Orthopaedic Institute, 301 East 17th Street, New York, N.Y. 10003.
§Department of Orthopaedic Surgery, The Hospital of the University of Pennsylvania, 3400 Spruce Street, Philadelphia, Pennsylvania 19104.
We performed a retrospective analysis of sixty-four consecutive patients who had had a resection arthroplasty of either the knee or the hip for the treatment of a deep infection and from whom specimens for intraoperative analysis of frozen sections had been obtained at the time of attempted prosthetic reimplantation. Three patients who had been managed with a resection arthroplasty for the treatment of a presumed deep infection and from whom specimens for intraoperative analysis of frozen sections had been obtained at the time of a second-stage reconstruction were excluded from this study because the presence of deep infection was not confirmed; in all three instances, the intraoperative cultures that were performed at the time of the resection arthroplasty were negative and permanent histological sections either were not prepared or had characteristics that were not consistent with a finding of acute inflammation.
All sixty-four patients were operated on at the Hospital for Joint Diseases Orthopaedic Institute between 1991 and 1997. The study group consisted of thirty-three women and thirty-one men, who had a mean age of sixty-four years (range, thirty-two to eighty-five years). Thirty-three patients had an infection at the site of a total knee arthroplasty; twenty-five, at the site of a total hip arthroplasty; and four, at the site of a hemiarthroplasty of the hip. Two patients had had previous open reduction and internal fixation of a hip fracture.
The infections developed at a mean of forty months (range, one to 187 months) after the previous operative procedure. The sixty-four patients had had a mean of two operations (range, one to five operations) on the involved hip or knee before the resection arthroplasty that was performed because of infection. Of the thirty-three total knee arthroplasties that were complicated by infection, twenty-five had been performed for the treatment of osteoarthritis; four, for the treatment of rheumatoid arthritis; three, for the treatment of posttraumatic osteoarthritis; and one, for the treatment of previous septic arthritis. Of the twenty-five total hip arthroplasties that were complicated by infection, twelve had been performed for the treatment of osteoarthritis; five, for the treatment of posttraumatic arthritis or a hip fracture; four, for the treatment of congenital dysplasia; two, for the treatment of osteonecrosis; one, for the treatment of psoriatic arthritis; and one, for the treatment of previous septic arthritis.
At the time of the resection arthroplasty, the implant (and the cement, if present) was removed, all tissues that appeared to be infected were thoroughly debrided, and the joint was copiously irrigated. An antibiotic-loaded cement spacer or beads were used in fifty-eight patients; 1.2 grams of tobramycin per package of cement was used for forty-four of these fifty-eight patients, 1.0 gram of vancomycin per package was used for two, and a combination of 1.2 grams of tobramycin and 1.0 gram of vancomycin per package was used for twelve.
Antibiotics were administered intravenously on the basis of the sensitivity profile of the infecting organism that was identified on intraoperative or preoperative culture. Antibiotic selection and postoperative therapy were monitored with the assistance of an infectious-disease consultant. All patients received a minimum of six weeks of intravenous antibiotic therapy. Organisms grown on culture of specimens obtained at the time of the resection arthroplasty included Staphylococcus epidermidis (twenty patients), Staphylococcus aureus (thirteen), Streptococcus viridans (seven), Escherichia coli (seven), Enterococcus faecalis (five), group-B Streptococcus (three), Streptococcus pneumoniae (one), and Enterobacter cloacae (one). One other patient had identification of multiple organisms, including Staphylococcus aureus, group-B Streptococcus, and Pseudomonas aeruginosa. The remaining six patients had negative findings on intraoperative culture of specimens obtained at the time of the resection arthroplasty; however, the findings on analysis of permanent histological sections were consistent with infection in all six.
The attempted reimplantation procedure or arthrodesis was performed at a mean of nineteen weeks (range, two to seventy-nine weeks) after the resection arthroplasty. Thirty-two patients were managed with a revision total knee arthroplasty with cement and thirty-one, with a revision total hip arthroplasty (twenty-six were managed with a femoral component inserted with cement and an acetabular component inserted without cement and five, with both components inserted without cement). The remaining patient had débridement of the knee at the time of the index operation because persistent infection was detected, and this patient subsequently was managed with an arthrodesis.
Tissue-sampling was performed according to a previously established protocol in which the pseudocapsule, granulation tissue, and other areas considered by the surgeon to be most suggestive of infection were biopsied routinely for histological analysis. Frozen sections of tissue were studied, after staining with hematoxylin and eosin, according to the following protocol: (1) granulation tissue was preferentially analyzed, although at times only dense fibrous or fibrin-rich tissue had been obtained and was therefore evaluated; (2) at least two samples of tissue were used; (3) the five most cellular fields (determined on the basis of the number of polymorphonuclear leukocytes) were analyzed; (4) polymorphonuclear leukocyte counts were performed under high-power (forty times) magnification in these five fields; and (5) only polymorphonuclear leukocytes, identified within tissue rather than fibrin, with well defined cytoplasmic borders were included in the count (cells with isolated nuclear fragmentation were excluded as they could not be definitely categorized as polymorphonuclear leukocytes). The frozen section was considered positive if a mean of ten polymorphonuclear leukocytes or more per high-power field were identified in the five most cellular fields that were examined.
After the frozen sections had been analyzed, permanent sections, between four and five micrometers thick, were prepared with use of paraffin-embedding and sectioning. These sections were analyzed according to the same criteria that had been used for the frozen sections. Swabs for culture (aerobic and anaerobic) were obtained from the same sites that had been analyzed histologically. Prophylactic perioperative antibiotics were withheld from all patients before collection of the intraoperative specimens for culture.
The results of the intraoperative analysis of the frozen sections, the analysis of the permanent histological sections, and the intraoperative cultures were compared. Although both agar plates and broth were used for the cultures, only growth on agar plates was considered a positive result. Persistent infection was defined as growth of an organism on culture that matched the original infecting organism or as findings on analysis of the permanent histological sections that were consistent with acute inflammation. The sensitivity, specificity, positive predictive value, negative predictive value, and accuracy were determined9.
Of the sixty-four patients, two had findings on intraoperative analysis of the frozen sections that were consistent with acute inflammation (that is, a mean of more than ten polymorphonuclear leukocytes were identified in the five most cellular fields). One of these two patients had positive findings on analysis of the permanent sections. The analysis of the frozen sections was considered to have yielded a false-positive result for the other patient, as the analysis of the permanent histological sections revealed a negative result and intraoperative cultures revealed no bacterial growth. Sixty-one of the sixty-two patients who were found to have fewer than ten polymorphonuclear leukocytes in the five most cellular fields on analysis of the frozen sections also had a negative result on analysis of the permanent histological sections (98 percent agreement). None of the analyses of the frozen sections revealed a mean of between five and nine polymorphonuclear cells in the five most cellular fields. Fifteen patients had a mean of fewer than five polymorphonuclear leukocytes in the five most cellular fields, and thus the criteria for acute inflammation were not met.
Four patients were considered to have an infection on the basis of positive intraoperative cultures or findings on analysis of the permanent histological sections that were consistent with acute inflammation. One of these patients was considered to have an infection because of growth of an organism on intraoperative culture that matched the original infecting organism and because of positive results on analysis of the permanent histological sections, one patient had the former finding only, and one had the latter finding only. The fourth patient, who had an infection with multiple organisms at the time of the resection arthroplasty, had growth of a different organism on culture at the time of the reoperation and also was considered to have a persistent infection. The remaining sixty patients had both negative intraoperative cultures and negative findings on analysis of the permanent histological sections.
Overall, fifty-nine of the analyses of frozen sections revealed true-negative results; three, false-negative results; one, a true-positive result; and one, a false-positive result. Thus, the analysis had a sensitivity of 25 percent (detection of one of four persistent infections), a specificity of 98 percent, a positive predictive value of 50 percent (one of two), a negative predictive value of 95 percent, and an accuracy of 94 percent.
Despite the general success of two-stage exchange arthroplasty in the treatment of deep periprosthetic infections of the hip and knee, some infections persist. Unfortunately, there are few algorithms for determining the suitability of a previously infected prosthetic site for reimplantation, and the decision to proceed with reimplantation often is made with use of subjective preoperative and intraoperative criteria, including the symptoms, the superficial appearance of the wound, and the gross intraoperative appearance of the tissue. Because of the implications of a failed two-stage exchange procedure for the patient, the surgeon, and the health-care system, improved diagnostic modalities are needed to avoid reimplantation into a tissue bed that still harbors active infection.
Many authors have recommended that the joint be aspirated before reimplantation of a total hip or knee prosthesis is attempted as part of a two-stage exchange protocol5,8,14,16,19,22,30-33. The ability of preoperative aspiration to identify persistent infection after resection arthroplasty and treatment with antibiotics in patients who have a deep infection has been analyzed specifically only by Cherney and Amstutz8, to our knowledge. In their series of thirty-three infected hips that were treated with a two-stage exchange protocol, cultures of preoperative aspirates from eight of the ten hips that subsequently became reinfected were negative. (The remaining two hips had not been aspirated before the reoperation.) Those authors concluded that preoperative aspiration was not a reliable method for identification of infection in that setting. Aspiration of the joint before a revision total joint arthroplasty generally has yielded substantial numbers of both false-positive and false-negative results, and its routine use remains controversial3,4,11,13,16,23,29.
Monitoring of the erythrocyte sedimentation rate and the C-reactive protein level also has been advocated13,19; however, these parameters (particularly the erythrocyte sedimentation rate) may remain falsely elevated in patients who have had recent operative intervention, and they are generally thought to be nonspecific1,6,17,28,29. Determination of the C-reactive protein level has been shown to be useful in monitoring a patient's response to antibiotic therapy24,28.
Similar difficulties have been encountered when nuclear medicine studies have been used to diagnose persistent infection after resection arthroplasty. Few studies have included patients who had a resection arthroplasty because of infection, and in those that have, these patients were not analyzed separately and were only a small percentage of the study population20. The only study that we are aware of that specifically examined the ability of indium-labeled leukocyte imaging to detect persistent infection after resection arthroplasty revealed a substantial number of false-positive results, which were attributed to persistent chronic inflammation secondary to the recent operative intervention26.
An association between the finding of acute inflammatory cells on histological examination and periprosthetic infection was first noted, to our knowledge, by Charosky et al.7, who recommended that intraoperative analysis of frozen sections be used to guide operative intervention at the time of revision total joint arthroplasty. The value of histological analysis and, specifically, intraoperative analysis of frozen sections was confirmed later by several authors2,12,18,21,22. Authors of previous studies have commented on the histological appearance of specimens obtained at the time of reoperation after resection arthroplasty8,15,16,25,30, and many have recommended that frozen sections be analyzed at the time of prosthetic reimplantation as part of a two-stage exchange protocol and have suggested that reimplantation not be undertaken if acute inflammation is observed10,15,16,25,30,32,33. There are scant data, however, related specifically to the reliability of intraoperative analysis of frozen sections in this situation.
Hughes et al.15 reported the findings of analysis of permanent histological sections of specimens obtained at the time of reimplantation of a hip prosthesis after twelve Girdlestone arthroplasties. They noted dense fibrous connective tissue with varying degrees of chronic inflammation in ten hips, granulation tissue in six, and only chronic inflammation in two. Three of the twelve hips had a recurrent infection; however, those authors found no association between the findings of histological analysis of tissue obtained at the time of the attempted reimplantation and the successful eradication of infection. Similarly, Cherney and Amstutz8 reported that, in their series of thirty-three infected hips that were treated with total arthroplasty after resection arthroplasty, eight had chronic inflammation or fibrosis on histological examination at the time of the reoperation. They also noted that the histological findings did not predict whether the infection had been eradicated.
Rand and Bryan25 reported the results of histological evaluation of synovial tissue obtained at the time of reimplantation from eleven of fourteen knees that were being treated with a two-stage exchange protocol because of failure of a total joint arthroplasty due to infection. They noted acute inflammation in six knees, acute and subacute inflammation in four, and no inflammation in one. Those authors did not comment on the relationship between the results of histological analysis and successful reimplantation. Insall et al.16 reported that, of eleven knees in which infection at the site of a total joint arthroplasty was treated with a two-stage exchange arthroplasty, nine were found to have chronic inflammation on analysis of permanent sections; the remaining two knees had both acute and chronic inflammation. After a mean of thirty-four months, no patient had a persistent infection; however, the degree of acute inflammation was not reported.
Walker and Schurman30 also recommended intraoperative analysis of frozen sections at the time of attempted prosthetic reimplantation after a resection arthroplasty performed because of infection. They noted a positive association between the results of frozen-section analysis and subsequent bacterial growth on intraoperative culture, but no specific data were presented. On the basis of their experience, they recommended that reimplantation be delayed if "more than a few polymorphonuclear cells per high-powered field" are seen.
The present study specifically addresses the reliability of intraoperative analysis of frozen sections in determining whether deep infection has been eradicated after resection arthroplasty and treatment with antibiotics. A major concern, before completion of the study, was that residual inflammation at the site of a recent operation would lead to a false-positive result. The findings of the present study allay this concern, as it appears that intraoperative histological analysis of frozen sections of specimens obtained after resection arthroplasty with adequate operative débridement and appropriate antibiotic therapy does reveal negative findings. Thus, even though there was one false-positive result on analysis of the frozen sections, the specificity of the test remained high at 98 percent.
Our results nevertheless suggest that analysis of frozen sections after resection arthroplasty and treatment with antibiotics is not as sensitive as an analysis performed at the time of an initial revision procedure2,12,18. Thus, although intraoperative analysis of frozen sections can be a useful adjunctive method for confirming the absence of infection in the setting described in the present study, the ability of this test to detect persistent infection is poor. The lower sensitivity in identifying active infection may be related to the relatively small number of our patients who had a persistent infection. In addition, the well known limitations of intraoperative analysis of frozen sections (particularly sampling error) are magnified in this situation, as only a small area of the joint may still harbor active infection and acute inflammation2,10,18. Furthermore, of the three false-negative results, two were for patients who had the second-stage reconstruction six weeks after the resection arthroplasty and were still receiving antibiotics intravenously. This suggests that the sensitivity of intraoperative analysis of frozen sections performed at the time of reoperation after resection arthroplasty may be decreased for patients who are receiving antibiotics.
Fifteen patients were found to have polymorphonuclear cells on intraoperative analysis of the frozen sections, but the number of cells was too low to meet the criterion for acute inflammation. Two of these patients were considered to have a persistent infection on the basis of positive findings on cultures or permanent histological sections. Thus, if a finding of any polymorphonuclear cells in the frozen section had been used as a criterion for acute inflammation, more persistent infections would have been detected. The sensitivity would have increased from 25 percent (detection of one of four persistent infections) to 75 percent (detection of three of four persistent infections). However, this would have led to eleven additional false-positive results, and the specificity of the test would have decreased from 98 to 80 percent. The accuracy of the test also would have decreased from 94 to 80 percent, with the surgeon potentially having been misled by the analysis of the frozen sections for thirteen as opposed to four patients. The results of this study show that an index of at least ten polymorphonuclear cells in the five most cellular fields led to the greatest number of correct diagnoses on the basis of intraoperative analysis of frozen sections. As no patient had a mean of between five and nine polymorphonuclear cells in the five most cellular fields at the time of the reoperation, we are unable to comment on the relative merits of use of an index of at least five as opposed to an index of at least ten as an indicator of infection in this setting. Because earlier data from our institution showed that the positive predictive value of intraoperative analysis of frozen sections is higher (with fewer false-positive results) with use of an index of more than ten than it is with use of an index of more than five, we continue to use the former index as our criterion for acute inflammation.
On the basis of our findings, we recommend that reimplantation be delayed if intraoperative analysis of frozen sections reveals a mean of more than ten polymorphonuclear cells in the five most cellular fields and that reimplantation be carried out if this analysis reveals a mean of less than ten polymorphonuclear cells in the five most cellular fields. We recognize, however, that this test may not detect all persistent infections. Intraoperative analysis of frozen sections after resection arthroplasty that is performed because of infection does not have the same sensitivity as has been documented for this technique when it has been used at the time of an initial revision procedure.
NOTE: The authors thank Walter Besser, M.D., Alan Dayan, M.D., Victor Frankel, M.D., Ronald Grelsamer, M.D., Frederick Jaffe, M.D., William Jaffe, M.D., Patrick Meere, M.D., and Steven Stuchin, M.D., for allowing the use of their patients' medical records in this study.
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